Making tadpole escape unpredictable: from behaviour to neurons
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1
University of Bristol, School of Biological Sciences, United Kingdom
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2
University of Edinburgh, Neuroinformatics Doctoral Training Centre, United Kingdom
Small young animals need to avoid being eaten and a widespread strategy to achieve this is to respond unpredictably [1]. We ask how the hatchling Xenopus frog tadpole, swims in an unpredictable direction? High-speed videos of young tadpoles show that touching the head skin evokes swimming that can start with a turn to either side (ca. 50:50%). Similar responses to head skin stimulation can be studied in immobilised tadpoles by recording motor nerve activity. A touch or stroke with a fine hair or a 0.1 ms current pulse to the head skin can evoke fictive swimming activity. As with the behaviour, the first motor response to this stimulation can be on either side of the animal (stimulated side: 49%, N = 10). It is also slightly asymmetrical as fictive swimming starts significantly earlier if it starts on the stimulated side (median 25 ms, N = 50) than when starting on the other side (35 ms, N = 41).
To uncover neuronal pathways initiating swimming, the hatchling tadpole offers a unique advantage: the excitatory reticulospinal neurons (dINs) which fire on every cycle and drive firing in all other 'swim' neurons have been characterized both anatomically and physiologically [2]. Initiation of swimming following head skin stimulation requires the activation of these neurons. We recently identified the neurons forming an ipsilateral pathway from trigeminal touch sensory neurons via trigeminal interneurons (tINs) to these reticulospinal dINs [3]. Paired whole-cell patch recordings are now being used to unravel the neurons responsible for bringing excitation also to the contralateral side. This gives us the opportunity to ask where and how the decisions to swim, and which side to turn to, are made in the CNS.
We propose that the dINs are multifunctional, decision-making, swim-gating and CPG-driving interneurons. When the head skin is stimulated, dINs on both sides are excited. If the dINs on one side are recruited as a group, they initiate flexion on that side followed by swimming. We propose that by chance, the excitation on one side will reach the threshold for this group activation of the dIN population first and then inhibit the other side, producing an unpredictable start side. Also, the dINs on the stimulated side receive excitation 7.5 ± 2.3 ms (mean ± SD) after the stimulus and spike after 18.8 ± 12.7 ms (N = 31) while the delays for excitation and spiking on the other side are longer (10.5 ± 1.6 ms and 34.4 ± 14.5 ms, N = 13). This difference corresponds well with the behavioural response, which is also later when starting on the unstimulated side. The protean nature of the dIN recruitment leads to protean turning behaviour with potential survival benefit. We are currently testing this hypothesis with neuronal network models.
References
[1] Domenici P, Blagburn JM, Bacon JP (2011) Animal escapology I: theoretical issues and emerging trends in escape trajectories. J Exp Biol 214:2463-2473
[2] Roberts A, Li W-C, Soffe SR (2010) How neurons generate behavior in a hatchling amphibian tadpole: an outline. Front Behav Neurosci 4:16
[3] Buhl E, Roberts A, Soffe SR (2012) The role of a trigeminal sensory nucleus in the initiation
of locomotion. J Physiol (in press)
Keywords:
Decision Making,
escape response,
initiation pathway,
Locomotion,
neuronal modelling,
reticulospinal neurons,
Trigeminal system,
Xenopus laevis
Conference:
Tenth International Congress of Neuroethology, College Park. Maryland USA, United States, 5 Aug - 10 Aug, 2012.
Presentation Type:
Poster (but consider for Participant Symposium)
Topic:
Sensorimotor Integration
Citation:
Buhl
E,
Soffe
SR,
Hull
M and
Roberts
A
(2012). Making tadpole escape unpredictable: from behaviour to neurons.
Conference Abstract:
Tenth International Congress of Neuroethology.
doi: 10.3389/conf.fnbeh.2012.27.00116
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Received:
25 Apr 2012;
Published Online:
07 Jul 2012.
*
Correspondence:
Dr. Edgar Buhl, University of Bristol, School of Biological Sciences, Bristol, Avon, BS8 1UG, United Kingdom, e.buhl@bristol.ac.uk